Open Access

Liquid biopsy for lung cancer immunotherapy (Review)

  • Authors:
    • Liang‑Liang Cai
    • Jie Wang
  • View Affiliations

  • Published online on: March 19, 2019     https://doi.org/10.3892/ol.2019.10166
  • Pages: 4751-4760
  • Copyright: © Cai et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )
Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )


Abstract

The recent successful use of the immune checkpoint inhibitors (CPIs) anti‑programmed death receptor‑1 (PD‑1)/PD‑1 ligand 1 in clinical trials indicates their crucial role in obtaining an effective cancer immune therapy. These CPIs have been identified to have an effective therapeutic response, particularly in tumors with high tumor mutation burden. Targeting private somatic mutations encoding immunogenic neoantigens (neo‑Ags) has been developed as an autologous gene therapy. T‑cell receptor‑engineered T cells targeting neo‑Ags are a novel option for adoptive cell therapy used for the treatment of lung cancer. However, not all patients experience an effective response from immunotherapy. Although the resistance mechanism of CPIs has been reported, its association with other treatment methods during systemic anticancer therapy remains unclear, particularly the treatment options following the emergence of drug resistance in lung cancer. The potential biomarkers used for liquid biopsy may assist in the identification of patients who would benefit the most from immunotherapy. Attempts to identify potential biomarkers for predicting clinical response to immunotherapy are underway. With regard to liquid biopsy, the present review summarizes and discusses the lung cancer management of immunotherapy for precision medicine by reviewing recent literature and associated clinical trials.

References

1 

Cameron F, Whiteside G and Perry C: Ipilimumab: First global approval. Drugs. 71:1093–1104. 2011. View Article : Google Scholar : PubMed/NCBI

2 

Hodi FS, Lawrence D, Lezcano C, Wu X, Zhou J, Sasada T, Zeng W, Giobbie-Hurder A, Atkins MB, Ibrahim N, et al: Bevacizumab plus ipilimumab in patients with metastatic melanoma. Cancer Immunol Res. 2:632–642. 2014. View Article : Google Scholar : PubMed/NCBI

3 

Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB, et al: Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med. 366:2443–2454. 2012. View Article : Google Scholar : PubMed/NCBI

4 

Wolchok JD, Kluger H, Callahan MK, Postow MA, Rizvi NA, Lesokhin AM, Segal NH, Ariyan CE, Gordon RA, Reed K, et al: Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med. 369:122–133. 2013. View Article : Google Scholar : PubMed/NCBI

5 

Larkin J, Chiarion-Sileni V, Gonzalez R, Grob JJ, Cowey CL, Lao CD, Schadendorf D, Dummer R, Smylie M, Rutkowski P, et al: Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N Engl J Med. 373:23–34. 2015. View Article : Google Scholar : PubMed/NCBI

6 

Borghaei H, Paz-Ares L, Horn L, Spigel DR, Steins M, Ready NE, Chow LQ, Vokes EE, Felip E, Holgado E, et al: Nivolumab versus docetaxel in advanced nonsquamous non-small-cell lung cancer. N Engl J Med. 373:1627–1639. 2015. View Article : Google Scholar : PubMed/NCBI

7 

Powles T, Eder JP, Fine GD, Braiteh FS, Loriot Y, Cruz C, Bellmunt J, Burris HA, Petrylak DP, Teng SL, et al: MPDL3280A (anti-PD-L1) treatment leads to clinical activity in metastatic bladder cancer. Nature. 515:558–562. 2014. View Article : Google Scholar : PubMed/NCBI

8 

Chen L and Han X: Anti-PD-1/PD-L1 therapy of human cancer: Past, present, and future. J Clin Invest. 125:3384–3391. 2015. View Article : Google Scholar : PubMed/NCBI

9 

Herbst RS, Soria JC, Kowanetz M, Fine GD, Hamid O, Gordon MS, Sosman JA, McDermott DF, Powderly JD, Gettinger SN, et al: Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature. 515:563–567. 2014. View Article : Google Scholar : PubMed/NCBI

10 

Garon EB, Rizvi NA, Hui R, Leighl N, Balmanoukian AS, Eder JP, Patnaik A, Aggarwal C, Gubens M, Horn L, et al: Pembrolizumab for the treatment of non-small-cell lung cancer. N Engl J Med. 372:2018–2028. 2015. View Article : Google Scholar : PubMed/NCBI

11 

Brahmer J, Reckamp KL, Baas P, Crino L, Eberhardt WE, Poddubskaya E, Antonia S, Pluzanski A, Vokes EE, Holgado E, et al: Nivolumab versus docetaxel in advanced squamous-cell non-small-cell lung cancer. N Engl J Med. 373:123–135. 2015. View Article : Google Scholar : PubMed/NCBI

12 

Rizvi NA, Mazieres J, Planchard D, Stinchcombe TE, Dy GK, Antonia SJ, Horn L, Lena H, Minenza E, Mennecier B, et al: Activity and safety of nivolumab, an anti-PD-1 immune checkpoint inhibitor, for patients with advanced, refractory squamous non-small-cell lung cancer (CheckMate 063): A phase 2, single-arm trial. Lancet Oncol. 16:257–265. 2015. View Article : Google Scholar : PubMed/NCBI

13 

Herbst RS, Baas P, Kim DW, Felip E, Perez-Gracia JL, Han JY, Molina J, Kim JH, Arvis CD, Ahn MJ, et al: Pembrolizumab versus docetaxel for previously treated, PD-L1-positive, advanced non-small-cell lung cancer (KEYNOTE-010): A randomised controlled trial. Lancet. 387:1540–1550. 2016. View Article : Google Scholar : PubMed/NCBI

14 

Borghaei H and Brahmer J: Nivolumab in nonsquamous non-small-cell lung cancer. N Engl J Med. 374:493–494. 2016.PubMed/NCBI

15 

Fehrenbacher L, Spira A, Ballinger M, Kowanetz M, Vansteenkiste J, Mazieres J, Park K, Smith D, Artal-Cortes A, Lewanski C, et al: Atezolizumab versus docetaxel for patients with previously treated non-small-cell lung cancer (POPLAR): A multicentre, open-label, phase 2 randomised controlled trial. Lancet. 387:1837–1846. 2016. View Article : Google Scholar : PubMed/NCBI

16 

Brahmer JR, Tykodi SS, Chow LQ, Hwu WJ, Topalian SL, Hwu P, Drake CG, Camacho LH, Kauh J, Odunsi K, et al: Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med. 366:2455–2465. 2012. View Article : Google Scholar : PubMed/NCBI

17 

Spigel DR, Schrock AB, Fabrizio D, Frampton GM, Sun J and He J: Total mutation burden (TMB) in lung cancer (LC) and relationship with response to PD-1/PD-L1 targeted therapies. Am Soc Clin Oncol. 2016. View Article : Google Scholar

18 

Anagnostou V, Smith KN, Forde PM, Niknafs N, Bhattacharya R, White J, Zhang T, Adleff V, Phallen J, Wali N, et al: Evolution of neoantigen landscape during immune checkpoint blockade in non-small cell lung cancer. Cancer Discov. 7:264–276. 2017. View Article : Google Scholar : PubMed/NCBI

19 

Vitale SG, Lagana AS, Capriglione S, Angioli R, La Rosa VL, Lopez S, Valenti G, Sapia F, Sarpietro G, Butticè S, et al: Target therapies for uterine carcinosarcomas: Current evidence and future perspectives. Int J Mol Sci. 18:E11002017. View Article : Google Scholar : PubMed/NCBI

20 

Bai H, Mao L, Wang HS, Zhao J, Yang L, An TT, Wang X, Duan CJ, Wu NM, Guo ZQ, et al: Epidermal growth factor receptor mutations in plasma DNA samples predict tumor response in Chinese patients with stages IIIB to IV non-small-cell lung cancer. J Clin Oncol. 27:2653–2659. 2009. View Article : Google Scholar : PubMed/NCBI

21 

Bai H, Wang Z, Chen K, Zhao J, Lee JJ, Wang S, Zhou Q, Zhuo M, Mao L, An T, et al: Influence of chemotherapy on EGFR mutation status among patients with non-small-cell lung cancer. J Clin Oncol. 30:3077–3083. 2012. View Article : Google Scholar : PubMed/NCBI

22 

Aparicio S and Caldas C: The implications of clonal genome evolution for cancer medicine. N Engl J Med. 368:842–851. 2013. View Article : Google Scholar : PubMed/NCBI

23 

Aguiar PN Jr, De Mello RA, Barreto CMN, Perry LA, Penny-Dimri J, Tadokoro H and Lopes GL Jr: Immune checkpoint inhibitors for advanced non-small cell lung cancer: Emerging sequencing for new treatment targets. ESMO Open. 2:e0002002017. View Article : Google Scholar : PubMed/NCBI

24 

Alexander W: European society for medical oncology 2016 congress. P T. 41:796–800. 2016.PubMed/NCBI

25 

Cyriac G and Gandhi L: Emerging biomarkers for immune checkpoint inhibition in lung cancer. Semin Cancer Biol. 52:269–277. 2018. View Article : Google Scholar : PubMed/NCBI

26 

Hegde PS, Karanikas V and Evers S: The where, the when, and the how of immune monitoring for cancer immunotherapies in the era of checkpoint inhibition. Clin Cancer Res. 22:1865–1874. 2016. View Article : Google Scholar : PubMed/NCBI

27 

Chen DS and Mellman I: Oncology meets immunology: The cancer-immunity cycle. Immunity. 39:1–10. 2013. View Article : Google Scholar : PubMed/NCBI

28 

Kim R, Emi M and Tanabe K: Cancer immunoediting from immune surveillance to immune escape. Immunology. 121:1–14. 2007. View Article : Google Scholar : PubMed/NCBI

29 

Bobisse S, Foukas PG, Coukos G and Harari A: Neoantigen-based cancer immunotherapy. Ann Transl Med. 4:2622016. View Article : Google Scholar : PubMed/NCBI

30 

Miller A, Asmann Y, Cattaneo L, Braggio E, Keats J, Auclair D, Lonial S; MMRF CoMMpass Network, ; Russell SJ and Stewart AK: High somatic mutation and neoantigen burden are correlated with decreased progression-free survival in multiple myeloma. Blood Cancer J. 7:e6122017. View Article : Google Scholar : PubMed/NCBI

31 

Turajlic S, Litchfield K, Xu H, Rosenthal R, McGranahan N, Reading JL, Wong YNS, Rowan A, Kanu N, Al Bakir M, et al: Insertion-and-deletion-derived tumour-specific neoantigens and the immunogenic phenotype: A pan-cancer analysis. Lancet Oncol. 18:1009–1021. 2017. View Article : Google Scholar : PubMed/NCBI

32 

Tran E, Robbins PF and Rosenberg SA: ‘Final common pathway’ of human cancer immunotherapy: Targeting random somatic mutations. Nat Immunol. 18:255–262. 2017. View Article : Google Scholar : PubMed/NCBI

33 

Tran E, Turcotte S, Gros A, Robbins PF, Lu YC, Dudley ME, Wunderlich JR, Somerville RP, Hogan K, Hinrichs CS, et al: Cancer immunotherapy based on mutation-specific CD4+ T cells in a patient with epithelial cancer. Science. 344:641–645. 2014. View Article : Google Scholar : PubMed/NCBI

34 

McGranahan N, Furness AJ, Rosenthal R, Ramskov S, Lyngaa R, Saini SK, Jamal-Hanjani M, Wilson GA, Birkbak NJ, Hiley CT, et al: Clonal neoantigens elicit T cell immunoreactivity and sensitivity to immune checkpoint blockade. Science. 351:1463–1469. 2016. View Article : Google Scholar : PubMed/NCBI

35 

Jenkins RW, Barbie DA and Flaherty KT: Mechanisms of resistance to immune checkpoint inhibitors. Br J Cancer. 118:9–16. 2018. View Article : Google Scholar : PubMed/NCBI

36 

McGranahan N and Swanton C: Clonal heterogeneity and tumor evolution: Past, present, and the future. Cell. 168:613–628. 2017. View Article : Google Scholar : PubMed/NCBI

37 

Reck M, Bondarenko I, Luft A, Serwatowski P, Barlesi F, Chacko R, Sebastian M, Lu H, Cuillerot JM and Lynch TJ: Ipilimumab in combination with paclitaxel and carboplatin as first-line therapy in extensive-disease-small-cell lung cancer: Results from a randomized, double-blind, multicenter phase 2 trial. Ann Oncol. 24:75–83. 2013. View Article : Google Scholar : PubMed/NCBI

38 

Forde PM, Chaft JE and Pardoll DM: Neoadjuvant PD-1 blockade in resectable lung cancer. N Engl J Med. 379:e142018. View Article : Google Scholar : PubMed/NCBI

39 

Samstein RM and Riaz N: The DNA damage response in immunotherapy and radiation. Adv Radiat Oncol. 3:527–533. 2018. View Article : Google Scholar : PubMed/NCBI

40 

Nakamura Y: Immunopharmacogenomics. Springer; Japan: pp. 4832015

41 

Schumacher TN and Scheper W: A liquid biopsy for cancer immunotherapy. Nat Med. 22:340–341. 2016. View Article : Google Scholar : PubMed/NCBI

42 

Heitzer E, Ulz P and Geigl JB: Circulating tumor DNA as a liquid biopsy for cancer. Clin Chem. 61:112–123. 2015. View Article : Google Scholar : PubMed/NCBI

43 

Cheng F, Su L and Qian C: Circulating tumor DNA: A promising biomarker in the liquid biopsy of cancer. Oncotarget. 7:48832–48841. 2016.PubMed/NCBI

44 

Akyuz N, Brandt A, Stein A, Schliffke S, Mahrle T, Quidde J, Goekkurt E, Loges S, Haalck T, Ford CT, et al: T-cell diversification reflects antigen selection in the blood of patients on immune checkpoint inhibition and may be exploited as liquid biopsy biomarker. Int J Cancer. 140:2535–2544. 2017. View Article : Google Scholar : PubMed/NCBI

45 

Gedvilaitė V, Schveigert D and Cicėnas S: Cell-free DNA in non-small cell lung cancer. Acta Med Litu. 24:138–144. 2017.PubMed/NCBI

46 

Mingari MC and Moretta L: Surface markers of human T lymphocytes. Ric Clin Lab. 12:439–448. 1982.PubMed/NCBI

47 

Gajewski TF: The next hurdle in cancer immunotherapy: Overcoming the Non-T-Cell-inflamed tumor microenvironment. Semin Oncol. 42:663–671. 2015. View Article : Google Scholar : PubMed/NCBI

48 

Sharma P and Allison JP: The future of immune checkpoint therapy. Science. 348:56–61. 2015. View Article : Google Scholar : PubMed/NCBI

49 

Inoue H, Park JH, Kiyotani K, Zewde M, Miyashita A, Jinnin M, Kiniwa Y, Okuyama R, Tanaka R, Fujisawa Y, et al: Intratumoral expression levels of PD-L1, GZMA, and HLA-A along with oligoclonal T cell expansion associate with response to nivolumab in metastatic melanoma. Oncoimmunology. 5:e12045072016. View Article : Google Scholar : PubMed/NCBI

50 

Duan J, Wang Y and Jiao S: Checkpoint blockade-based immunotherapy in the context of tumor microenvironment: Opportunities and challenges. Cancer Med. 7:4517–4529. 2018. View Article : Google Scholar : PubMed/NCBI

51 

Alexandrov LB, Nik-Zainal S, Wedge DC, Aparicio SA, Behjati S, Biankin AV, Bignell GR, Bolli N, Borg A, Børresen-Dale AL, et al: Signatures of mutational processes in human cancer. Nature. 500:415–421. 2013. View Article : Google Scholar : PubMed/NCBI

52 

Kandoth C, McLellan MD, Vandin F, Ye K, Niu B, Lu C, Xie M, Zhang Q, McMichael JF, Wyczalkowski MA, et al: Mutational landscape and significance across 12 major cancer types. Nature. 502:333–339. 2013. View Article : Google Scholar : PubMed/NCBI

53 

Kinoshita Y, Ishiguro T, Sano Y, Azuma Y, Tsunenari T, Ono N, Kayukawa Y, Ueda O, Wada NA, Hino H, et al: Anti-GPC3 TRAB, a first-in-class T cell-redirecting bispecific antibody targeting glypican-3 with potent in vitro and in vivo antitumor efficacy against solid tumors. Cancer Research. 76:14822016. View Article : Google Scholar

54 

Teng MW, Ngiow SF, Ribas A and Smyth MJ: Classifying Cancers Based on T-cell Infiltration and PD-L1. Cancer Res. 75:2139–2145. 2015. View Article : Google Scholar : PubMed/NCBI

55 

Smyth MJ, Ngiow SF, Ribas A and Teng MW: Combination cancer immunotherapies tailored to the tumour microenvironment. Nat Rev Clin Oncol. 13:143–158. 2016. View Article : Google Scholar : PubMed/NCBI

56 

Konishi J, Yamazaki K, Azuma M, Kinoshita I, Dosaka-Akita H and Nishimura M: B7-H1 expression on non-small cell lung cancer cells and its relationship with tumor-infiltrating lymphocytes and their PD-1 expression. Clin Cancer Res. 10:5094–5100. 2004. View Article : Google Scholar : PubMed/NCBI

57 

Kawai O, Ishii G, Kubota K, Murata Y, Naito Y, Mizuno T, Aokage K, Saijo N, Nishiwaki Y, Gemma A, et al: Predominant infiltration of macrophages and CD8(+) T Cells in cancer nests is a significant predictor of survival in stage IV nonsmall cell lung cancer. Cancer. 113:1387–1395. 2008. View Article : Google Scholar : PubMed/NCBI

58 

Mu CY, Huang JA, Chen Y, Chen C and Zhang XG: High expression of PD-L1 in lung cancer may contribute to poor prognosis and tumor cells immune escape through suppressing tumor infiltrating dendritic cells maturation. Med Oncol. 28:682–688. 2011. View Article : Google Scholar : PubMed/NCBI

59 

He Y, Yu H, Rozeboom L, Rivard CJ, Ellison K, Dziadziuszko R, Suda K, Ren S, Wu C, Hou L, et al: LAG-3 protein expression in non-small cell lung cancer and its relationship with PD-1/PD-L1 and tumor-infiltrating lymphocytes. J Thorac Oncol. 12:814–823. 2017. View Article : Google Scholar : PubMed/NCBI

60 

Zhang Y, Cai P, Liang T, Wang L and Hu L: TIM-3 is a potential prognostic marker for patients with solid tumors: A systematic review and meta-analysis. Oncotarget. 8:31705–31713. 2017.PubMed/NCBI

61 

Liu XG, Hou M and Liu Y: TIGIT, a novel therapeutic target for tumor immunotherapy. Immunol Invest. 46:172–182. 2017. View Article : Google Scholar : PubMed/NCBI

62 

Anderson AC, Joller N and Kuchroo VK: Lag-3, Tim-3, and TIGIT: Co-inhibitory receptors with specialized functions in immune regulation. Immunity. 44:989–1004. 2016. View Article : Google Scholar : PubMed/NCBI

63 

Koyama S, Akbay EA, Li YY, Herter-Sprie GS, Buczkowski KA, Richards WG, Gandhi L, Redig AJ, Rodig SJ, Asahina H, et al: Adaptive resistance to therapeutic PD-1 blockade is associated with upregulation of alternative immune checkpoints. Nat Commun. 7:105012016. View Article : Google Scholar : PubMed/NCBI

64 

Gros A, Parkhurst MR, Tran E, Pasetto A, Robbins PF, Ilyas S, Prickett TD, Gartner JJ, Crystal JS, Roberts IM, et al: Prospective identification of neoantigen-specific lymphocytes in the peripheral blood of melanoma patients. Nat Med. 22:433–438. 2016. View Article : Google Scholar : PubMed/NCBI

65 

Nicolazzo C, Raimondi C, Mancini M, Caponnetto S, Gradilone A, Gandini O, Mastromartino M, Del Bene G, Prete A, Longo F, et al: Monitoring PD-L1 positive circulating tumor cells in non-small cell lung cancer patients treated with the PD-1 inhibitor Nivolumab. Sci Rep. 6:317262016. View Article : Google Scholar : PubMed/NCBI

66 

Hellmann MD, Ciuleanu TE, Pluzanski A, Lee JS, Otterson GA, Audigier-Valette C, Minenza E, Linardou H, Burgers S, Salman P, et al: Nivolumab plus ipilimumab in lung cancer with a high tumor mutational burden. N Engl J Med. 378:2093–2104. 2018. View Article : Google Scholar : PubMed/NCBI

67 

Gandara DR, Paul SM, Kowanetz M, Schleifman E, Zou W, Li Y, Rittmeyer A, Fehrenbacher L, Otto G, Malboeuf C, et al: Blood-based tumor mutational burden as a predictor of clinical benefit in non-small-cell lung cancer patients treated with atezolizumab. Nat Med. 24:1441–1448. 2018. View Article : Google Scholar : PubMed/NCBI

68 

Gandara DR, Kowanetz M, Mok TSK, Rittmeyer A, Fehrenbacher L, Fabrizio D, Otto G, Malboeuf C, Lieber D, Paul SM, et al: 1295OBlood-based biomarkers for cancer immunotherapy: Tumor mutational burden in blood (bTMB) is associated with improved atezolizumab (atezo) efficacy in 2L+ NSCLC (POPLAR and OAK). Ann Oncol. 28 (Suppl 5):2017. View Article : Google Scholar

69 

Rosenberg SA and Restifo NP: Adoptive cell transfer as personalized immunotherapy for human cancer. Science. 348:62–68. 2015. View Article : Google Scholar : PubMed/NCBI

70 

Rizvi NA, Hellmann MD, Snyder A, Kvistborg P, Makarov V, Havel JJ, Lee W, Yuan J, Wong P, Ho TS, et al: Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science. 348:124–128. 2015. View Article : Google Scholar : PubMed/NCBI

71 

Durgeau A, Virk Y, Corgnac S and Mami-Chouaib F: Recent advances in targeting CD8 T-Cell immunity for more effective cancer immunotherapy. Front Immunol. 9:142018. View Article : Google Scholar : PubMed/NCBI

72 

Pasetto A, Gros A, Robbins PF, Deniger DC, Prickett TD, Matus-Nicodemos R, Douek DC, Howie B, Robins H, Parkhurst MR, et al: Tumor-and neoantigen-reactive T-cell receptors can be identified based on their frequency in fresh tumor. Cancer Immunol Res. 4:734–743. 2016. View Article : Google Scholar : PubMed/NCBI

73 

Bassani-Sternberg M and Coukos G: Mass spectrometry-based antigen discovery for cancer immunotherapy. Curr Opin Immunol. 41:9–17. 2016. View Article : Google Scholar : PubMed/NCBI

74 

Caron E, Kowalewski DJ, Chiek Koh C, Sturm T, Schuster H and Aebersold R: Analysis of major histocompatibility complex (MHC) immunopeptidomes using mass spectrometry. Mol Cell Proteomics. 14:3105–3117. 2015. View Article : Google Scholar : PubMed/NCBI

75 

Khodadoust MS, Olsson N, Wagar LE, Haabeth OA, Chen B, Swaminathan K, Rawson K, Liu CL, Steiner D, Lund P, et al: Antigen presentation profiling reveals recognition of lymphoma immunoglobulin neoantigens. Nature. 543:723–727. 2017. View Article : Google Scholar : PubMed/NCBI

76 

Cai LL, Ye HM, Zheng LM, Ruan RS and Tzeng CM: Circulating tumor cells (CTCs) as a liquid biopsy material and drug target. Curr Drug Targets. 15:965–972. 2014.PubMed/NCBI

77 

Rizvi NA, Hellmann MD, Brahmer JR, Juergens RA, Borghaei H, Gettinger S, Chow LQ, Gerber DE, Laurie SA, Goldman JW, et al: Nivolumab in combination with platinum-based doublet chemotherapy for first-line treatment of advanced non-small-cell lung cancer. J Clin Oncol. 34:2969–2979. 2016. View Article : Google Scholar : PubMed/NCBI

78 

Liu SY and Wu YL: Ongoing clinical trials of PD-1 and PD-L1 inhibitors for lung cancer in China. J Hematol Oncol. 10:1362017. View Article : Google Scholar : PubMed/NCBI

79 

Motzer RJ, Escudier B, McDermott DF, George S, Hammers HJ, Srinivas S, Tykodi SS, Sosman JA, Procopio G, Plimack ER, et al: Nivolumab versus everolimus in advanced renal-cell carcinoma. N Engl J Med. 373:1803–1813. 2015. View Article : Google Scholar : PubMed/NCBI

80 

Robert C, Long GV, Brady B, Dutriaux C, Maio M, Mortier L, Hassel JC, Rutkowski P, McNeil C, Kalinka-Warzocha E, et al: Nivolumab in previously untreated melanoma without BRAF mutation. N Engl J Med. 372:320–330. 2015. View Article : Google Scholar : PubMed/NCBI

81 

Ribas A, Puzanov I, Dummer R, Schadendorf D, Hamid O, Robert C, Hodi FS, Schachter J, Pavlick AC, Lewis KD, et al: Pembrolizumab versus investigator-choice chemotherapy for ipilimumab-refractory melanoma (KEYNOTE-002): A randomised, controlled, phase 2 trial. Lancet Oncol. 16:908–918. 2015. View Article : Google Scholar : PubMed/NCBI

82 

Chen Q, Li T and Yue W: Drug response to PD-1/PD-L1 blockade: Based on biomarkers. Onco Targets Ther. 11:4673–4683. 2018. View Article : Google Scholar : PubMed/NCBI

83 

Koeppel F, Blanchard S, Jovelet C, Genin B, Marcaillou C, Martin E, Rouleau E, Solary E, Soria JC, André F and Lacroix L: Whole exome sequencing for determination of tumor mutation load in liquid biopsy from advanced cancer patients. PLoS One. 12:e01881742017. View Article : Google Scholar : PubMed/NCBI

84 

Ilie M, Khambata-Ford S, Copie-Bergman C, Huang L, Juco J, Hofman V and Hofman P: Use of the 22C3 anti-PD-L1 antibody to determine PD-L1 expression in multiple automated immunohistochemistry platforms. PLoS One. 12:e01830232017. View Article : Google Scholar : PubMed/NCBI

85 

Marchetti A, Barberis M, Franco R, De Luca G, Pace MV, Staibano S, Volante M, Buttitta F, Guerini-Rocco E, Righi L, et al: Multicenter comparison of 22c3 pharmDx (Agilent) and SP263 (Ventana) assays to test PD-L1 expression for NSCLC patients to be treated with immune checkpoint inhibitors. J Thoracic Oncol. 12:1654–1663. 2017. View Article : Google Scholar

86 

Kowanetz M, Koeppen H, Zou W, Mariathasan S, Hellmann M, Kockx M, Chappey C, Kadel E, Smith D, Miley N, et al: Abstract A017: PD-L1 as a predictive biomarker for atezolizumab (MPDL3280A; anti-PDL1) in non-small cell lung cancer (NSCLC). AACR. 2016.

87 

Hu X and Hay JW: First-line pembrolizumab in PD-L1 positive non-small-cell lung cancer: A cost-effectiveness analysis from the UK health care perspective. Lung Cancer. 123:166–171. 2018. View Article : Google Scholar : PubMed/NCBI

88 

Dang TO, Ogunniyi A, Barbee MS and Drilon A: Pembrolizumab for the treatment of PD-L1 positive advanced or metastatic non-small cell lung cancer. Expert Rev Anticancer Ther. 16:13–20. 2016. View Article : Google Scholar : PubMed/NCBI

89 

Ibrahim RA, Berman DM, Depril V, Humphrey RW, Chen T and Messina M: Ipilimumab safety profile: Summary of findings from completed trials in advanced melanoma. J Clin Oncol. 29 (15-Suppl):85832011. View Article : Google Scholar

90 

Teply BA and Lipson EJ: Identification and management of toxicities from immune checkpoint-blocking drugs. Oncology (Williston Park). 3 (28 Suppl):30–38. 2014.

91 

Efremova M, Finotello F, Rieder D and Trajanoski Z: Neoantigens generated by individual mutations and their role in cancer immunity and immunotherapy. Front Immunol. 8:16792017. View Article : Google Scholar : PubMed/NCBI

92 

Wilson EA and Anderson KS: Lost in the crowd: Identifying targetable MHC class I neoepitopes for cancer immunotherapy. Expert Rev Proteomics. 15:1065–1077. 2018. View Article : Google Scholar : PubMed/NCBI

93 

Bassani-Sternberg M, Bräunlein E, Klar R, Engleitner T, Sinitcyn P, Audehm S, Straub M, Weber J, Slotta-Huspenina J, Specht K, et al: Direct identification of clinically relevant neoepitopes presented on native human melanoma tissue by mass spectrometry. Nat Commun. 7:134042016. View Article : Google Scholar : PubMed/NCBI

94 

Klebanoff CA, Rosenberg SA and Restifo NP: Prospects for gene-engineered T cell immunotherapy for solid cancers. Nat Med. 22:26–36. 2016. View Article : Google Scholar : PubMed/NCBI

95 

Politi K and Herbst RS: Lung cancer in the era of precision medicine. Clin Cancer Res. 21:2213–2220. 2015. View Article : Google Scholar : PubMed/NCBI

96 

Ramalingam S, Hui R, Gandhi L, Carcereny E, Felip E, Ahn MJ, Eder JP, Balmanoukian AS, Leighl N, Aggarwal C, et al: P2. 39: Long-Term OS for patients with advanced NSCLC enrolled in the KEYNOTE-001 study of pembrolizumab. J Thoracic Oncol. 11:S241–S242. 2016. View Article : Google Scholar

97 

Gettinger S, Rizvi NA, Chow LQ, Borghaei H, Brahmer J, Ready N, Gerber DE, Shepherd FA, Antonia S, Goldman JW, et al: Nivolumab monotherapy for first-line treatment of advanced non-small-cell lung cancer. J Clin Oncol. 34:2980–2987. 2016. View Article : Google Scholar : PubMed/NCBI

98 

Forde PM, Smith KN, Chaft JE, Hellmann M, Merghoub T, Wolchok JD, Yang SC, Battafarano RJ, Gabrielson E, Georgiades CS, et al: NSCLC, early stageNeoadjuvant anti-PD1, nivolumab, in early stage resectable non-small-cell lung cancer. Ann Oncol. 27 (Suppl 6):LBA41–PR. 2016. View Article : Google Scholar

99 

Antonia S, Rizvi N, Brahmer JR, Ou SHL, Khleif SN, Hwu WJ, Gutierrez M, Schoffski P, Hamid O, Weiss J, et al: Abstract A047: Safety and clinical activity of durvalumab (MEDI4736), an anti-programmed cell death ligand-1 (PD-L1) antibody, in patients with non-small cell lung cancer (NSCLC). AACR. 2016.

Related Articles

Journal Cover

June 2019
Volume 17 Issue 6

Print ISSN: 1792-1074
Online ISSN:1792-1082

Sign up for eToc alerts

Recommend to Library

Copy and paste a formatted citation
APA
Cai, L., & Cai, L. (2019). Liquid biopsy for lung cancer immunotherapy (Review). Oncology Letters, 17, 4751-4760. https://doi.org/10.3892/ol.2019.10166
MLA
Cai, L., Wang, J."Liquid biopsy for lung cancer immunotherapy (Review)". Oncology Letters 17.6 (2019): 4751-4760.
Chicago
Cai, L., Wang, J."Liquid biopsy for lung cancer immunotherapy (Review)". Oncology Letters 17, no. 6 (2019): 4751-4760. https://doi.org/10.3892/ol.2019.10166